Zoological Studies 51(4): 429-441 (2012)

Attractiveness of Different Bait to the Scarabaeinae (Coleoptera: ) in Forest Fragments in Extreme Southern Brazil Pedro Giovâni da Silva1,*, Fernando Z. Vaz-de-Mello2, and Rocco Alfredo Di Mare1 1Programa de Pós-Graduação em Biodiversidade , Univ. Federal de Santa Maria, Avenida Roraima, 1000, Camobi, CEP 97105- 900, Santa Maria, Rio Grande do Sul, Brazil 2Instituto de Biociências, Departamento de Biologia e Zoologia, Univ. Federal de Mato Grosso, Avenida Fernando Corrêa da Costa, 2367, Boa Esperança, CEP 78060-900, Cuiabá, Mato Grosso, Brazil

(Accepted December 9, 2011)

Pedro Giovâni da Silva, Fernando Z. Vaz-de-Mello, and Rocco Alfredo Di Mare (2012) Attractiveness of different bait to the Scarabaeinae (Coleoptera: Scarabaeidae) in forest fragments in extreme southern Brazil. Zoological Studies 51(4): 429-441. The aim of this study was to investigate the attractiveness of different types of bait to the Scarabaeinae. Scarabaeinae fauna was sampled using pitfall traps in 3 forest fragments of Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and Apr. 2010. Each received 27 traps placed on 3 transects, each containing 3 sets of 3 traps, respectively baited with human excrement, rotten meat, and rotten banana. Of the total number of species and individuals collected, 33 species and 75.02% of individuals were attracted to human excrement, 29 species and 20.26% of individuals to meat, and only 25 species and 4.72% of individuals to the banana. Kruskal-Wallis tests showed significant statistical differences among the mean (H = 20.65, d.f. = 2, p < 0.01) and abundance (H = 21.56, d.f. = 2, p < 0.01) of beetles attracted to each bait type. An ordination analysis showed the formation of different groups according to feeding habits and trophic niche overlap. According to Levins’ index, 14 species were coprophagous, 13 were generalists, and 2 necrophagous. Differences found occurred due to the great change in dung assemblages from each type of baited trap during the study period. In this study, human feces was the most attractive bait, differing significantly from carrion and rotten banana in both species richness and of the Scarabaeinae. http://zoolstud.sinica.edu.tw/Journals/51.4/429.pdf

Key words: Dung , Trophic , Coprophagy, Necrophagy, Saprophagy.

The subfamily Scarabaeinae (Coleoptera: Apparently, the Scarabaeinae evolved Scarabaeidae) includes dung beetles, a globally from saprophagous ancestors, which lived in distributed group of -feeding , which Afrotropical forests at the Mesozoic-Cenozoic contribute to important ecological functions, such boundary (~65 million years ago [Mya]) (Cambefort as nutrient recycling, secondary seed dispersal, 1991, Gill 1991, Halffter 1991, Davis et al. 2002, bioturbation, and natural control of cattle parasites Monaghan et al. 2007, Halffter and Halffter (Nichols et al. 2008). These beetles mainly eat 2009). Their great global diversification seems mammal feces (coprophagy), carrion (necrophagy), to have followed the increase in mammal dung and rotting plant matter (saprophagy), and they types during the Cenozoic, which would have may be specialists or generalists (Halffter and influenced the high specialization of the group to Matthews 1966, Halffter and Edmonds 1982, coprophagy (Cambefort 1991, Davis et al. 2002, Hanski and Cambefort 1991, Halffter and Halffter Monaghan et al. 2007, Arillo and Ortuño 2008, 2009). Davis 2009, Sole and Scholtz 2010, Philips 2011).

*To whom correspondence and reprint requests should be addressed. Current address: Programa de Pós-Graduação em Ecologia, Departamento de Ecologia e Zoologia, Univ. Federal de Santa Catarina, CEP 88040-900, Florianópolis, Santa Catarina, Brazil. E-mail:[email protected]

429 430 Silva et al. – Attractiveness of Different Baits to the Scarabaeinae

Necrophagy in the Neotropical Scarabaeinae may tropical forests (Halffter and Matthews 1966), the be linked to reduced dung resources owing to relationship of dung beetles with the mammalian mass extinctions of mammal megafauna between fauna (and its feces) is also expected in the the Pliocene and Pleistocene (5-2 Mya) (Halffter subtropics. and Matthews 1966, Halffter 1991). Although With reference to the evolutionary ecolo- saprophagy is currently the preferred eating habit gical origins of the subfamily, the current paper of some species (Halffter and Halffter 2009), it examines trophic associations of the scarabaeine was hypothesized to have resurfaced as a new fauna of 3 subtropical forest fragments in behavior, different from primitive saprophagy southern Brazil using 3 principal food types: (Cambefort 1991, Halffter and Halffter 2009). plant matter (represented by rotten bananas), The ingestion of decaying plant material is an dung (represented by human feces), and carrion alternative diet which may promote a decrease (represented by rotten chicken offal). in among species, especially within forests. However, coprophagy is the predominant current feeding habit of dung beetles, followed by MATERIALS AND METHODS necrophagy (Halffter and Matthews 1966, Halffter and Edmonds 1982, Hanski and Cambefort 1991, Study area Simmons and Ridsdill-Smith 2011). The current range of trophic niches occupied The municipality of Santa Maria is located by scarabaeine species would reflect the wide in the central region of Rio Grande do Sul, Brazil availability of different food resources available (Fig. 1). It lies in the transition zone between the throughout their evolution, since there are species ‘Depressão Central’ and the ‘Planalto Meridional associated with other resources. These include Brasileiro’ (Southern Brazilian Plateau) at the edge fungi (Halffter and Matthews 1966, Navarrete- of the Atlantic Forest and Pampa biomes (IBGE Heredia and Galindo-Miranda 1997, Falqueto 2010). The city is typified by grassland areas and et al. 2005), rotten eggs (Louzada and Vaz- deciduous seasonal forest vegetation belonging to de-Mello 1997, Pfrommer and Krell 2004), and the ‘Fralda da Serra Geral’ (Pereira et al. 1989), even on other (Pereira and variously situated on floodplains, lowlands, and Martínez 1956, Hertel and Colli 1998, Larsen et mountains, with elevations ranging 40-500 m. The al. 2006 2009, Silveira et al. 2006). climate is hot, wet, and subtropical of type Cfa complexity, a high diversity of mammals (and their according to the Köppen-Geiger classification (Pell feces), past inter- and intraspecific competition, et al. 2007). The annual precipitation averages and the availability of other food resources during around 1700 mm, with rainfall well distributed the evolutionary history of the Scarabaeinae may throughout the year (Pereira et al. 1989). The have been some of the factors that led species average annual temperature is approximately to develop food alternatives which differ from the 19°C, with minima varying between 8 and 10°C, ancestral diet (Gill 1991, Halffter 1991, Hanski and maxima between 32 and 40°C, and frequent frost Cambefort 1991, Monaghan et al. 2007). in winter (Nimer 1990). The current worldwide distribution of dung In order to conduct the present and other beetles is strongly influenced by the diversity of studies, species of the Scarabaeinae were mammal dung and climate (Davis and Scholtz sampled in 3 non-contiguous forest fragments of 2001, Davis et al. 2002) with the tropical region different sizes and levels of anthropic . having a high diversity of the Scarabaeinae (Halffter They are identified as follows. and Matthews 1966, Hanski and Cambefort 1991, 1) Morro do Elefante (29°40'33"S, 53°43' Davis et al. 2002). In the Neotropical Region, 14"W) is an around 730-ha, non-isolated area of scarabaeine species richness is primarily centered deciduous seasonal forest of the scarp of ‘Planalto on forests and differs from the Afrotropical fauna Médio Riograndense’ (Rio Grande do Sul Medium which shows greater diversity in savannas, Plateau) or of ‘Fralda da Serra Geral’ (Machado although species richness of each is related to and Longhi 1990). On its southern edge, there are the diversity of excrement provided by vertebrates some small plantations of Pinus spp., Eucalyptus present in the in their respective spp., and Citrus spp., and a few trails and glades. regions (Gill 1991, Halffter 1991, Davis et al. Its surroundings are characterized by fields, 2002). Although subtropical forests possess agricultural plantations, and a sequence of other a smaller number of scarabaeine species than mountains with similar forest vegetation. Based on Zoological Studies 51(4): 429-441 (2012) 431 the classification by Silva (2011b), it is regarded as 2003, Spector 2006). a fragment with a high level of preservation. A trap consisted of a 1000-ml plastic 2) Morro do Cerrito (29°42'07"S, 53°47'08"W) container, 13 cm in diameter and 10 cm deep, is a 140-ha isolated area of deciduous seasonal which was buried so that its rim was at ground level forest of ‘Serra Geral’ belonging to the ‘Depressão (Lobo et al. 1988, Ausden 1996). To accomm- Central’ of Rio Grande do Sul (Pereira et al. odate the bait, a smaller plastic pot was placed 1989). It has areas of glades, exotic trees, and into the larger container. A solution of water buildings and is largely surrounded by housing and (350 ml), formalin (10%), and detergent was put a number of similar but smaller forest fragments. inside the trap. The study was conducted between Based on the classification by Silva (2011b), it is 1 May 2009 and 30 Apr. 2010, encompassing the considered a forest fragment with an intermediate 4 seasons of the year (winter, 21 June to 21 Sept.; level of preservation. spring, 22 Sept. to 20 Dec.; summer, 21 Dec. to 20 3) Campus of Univ. Federal de Santa Maria Mar.; and autumn, 21 Mar. to 20 June). Collections (29°43'27"S, 53°43'29"W) is a 53-ha forest fra- took place in 2-wk periods, in the middle and gment with secondary native vegetation in the end of each month, totaling 24 samplings. Traps understory encompassed by a mixed plantations remained at the study sites during the entire of Pinus spp. and Eucalyptus spp., which replaced period, and the bait was periodically renewed. areas of grassland and riparian vegetation nearly Traps were baited with human feces (20 g), 30 yr ago (Soares and Costa 2001, Dambros et chicken organs (40 g), or bananas (50 g). The 2 al. 2004, Madruga et al. 2007). It is surrounded latter bait types were allowed to rot for 3 d at room by grasslands, agricultural plantations, a few temperature before use. Such bait represents buildings, and some similar neighboring forest the 3 major trophic guilds of these insects: fragments. This habitat is considered to have a coprophagy, necrophagy, and saprophagy (Halffter high level of disturbance due to the presence of and Matthews 1966). exotic trees and the great transformation of the In total, 27 traps were installed in each frag- fragment and its surroundings (Silva 2011b). ment, arranged in 3 transects. Transects were Monthly temperature and precipitation data separated from one another by 100 m and were obtained from the meteorological station of contained 3 sets of 3 traps, each set separated Univ. Federal de Santa Maria, Santa Maria, Brazil. by 30 m. Each set of 3 traps was arranged in a triangular shape with each trap separated by 2 m Sampling method and baited with one of the 3 kinds of bait in order to enable the selection of a by the beetles Individuals of the Scarabaeinae were (Almeida and Louzada 2009). captured using baited pitfall traps. This is Separate beetle samples are stored at considered the most efficient sampling method for the Laboratory of Evolutionary Biology at Univ. collecting the majority of this group (Lobo et al. Federal de Santa Maria (UFSM). They were first 1988, Halffter and Favila 1993, Milhomem et al. identified to the generic and subgeneric levels

70°00'W 45°00'W 53°00'W 54°52'W (A) (B) (C) N 28°00'S

1 2 3 15°00'S 29°47'S

32°00'S

1500 km 250 km 20 km 30°00'S

Fig. 1. Location of 3 in Santa Maria (C), Rio Grande do Sul (B), Brazil (A), sampled for species of the Scarabaeinae between May 2009 and Apr. 2010, using pitfall traps baited with human excrement, rotten meat, and rotten banana. Forest fragments sampled: ‘Morro do Elefante’ (1), ‘Morro do Cerrito’ (2), and ‘Campus of Univ. Federal de Santa Maria (3). 432 Silva et al. – Attractiveness of Different Baits to the Scarabaeinae using a dichotomous key for the Scarabaeinae of was used to determine differences in abundance the Americas (Vaz-de-Mello et al. 2011), and their and richness of the Scarabaeinae throughout identification was subsequently confirmed by the the seasons of the year on the different kinds of 2nd author. Voucher specimens are deposited in bait. Here, collections were arranged according to the collections of UFSM and at Univ. Federal de each seasonal period. In order to homogenize the Mato Grosso (UFMT). variance, the data were square root-transformed. Normality was checked by Shapiro-Wilk tests in Data analysis the program PAST 2.02.

The proximity of the pitfall traps allowed dung beetles to choose between traps baited with RESULTS different food types (i.e., a cafeteria experiment, see Almeida and Louzada 2009). The trophic In total, 33 species were recorded with 25 guild of each species was inferred using Levins’ species (75.75%) attracted to all 3 bait types. Of standardized index of niche breadth (BA) (Levins the total number of individuals collected (19,699), 1968, Krebs 1999) for species with an abundance 75.02% were attracted to human feces, 20.26% of > 15 individuals. This index is scaled from 0 to 1, to rotten meat, and 4.72% to fermented banana. and the greater the value, the greater the degree All 33 of the species were attracted to human of trophic generalization of the species. Species feces (Table 1), where Canthidium aff. trinodosum were classified into coprophagous, necrophagous, (Boheman, 1858) (27.49%), Dichotomius assifer or saprophagous specialists when the Levins’ (Eschscholtz, 1822) (19.07%), and Canthon latipes index was ≤ 0.5, and as generalists when the value Blanchard, 1845 (17.44%) were the most abundant of the index was higher (Krebs 1999, Filgueiras species. In traps baited with rotten meat, 29 et al. 2009). The simplified index of Morisita- species were captured, where C. aff. trinodosum Horn (IMH) (Horn 1966) was used to determine (16.58%), C. latipes (13.88%), and Canthon lividus the degree of niche overlap in food resource use Blanchard, 1845 (10.57%) were the most abundant by scarabaeine species. These indices were species. In traps baited with rotten banana, 25 calculated using Ecological Methodology software species were collected, and C. aff. trinodosum (Kenney and Krebs 2000). (21.44%), Canthidium aff. dispar Harold, 1867 Ordination analyses were conducted to (1) (14.26%), and C. latipes (10.72%) were the most determine temporal differences in the association abundant species. Kruskal-Wallis tests showed of scarabaeine assemblages with different bait significant statistical differences in the average types, and (2) verify the degree of specialization species richness (H = 20.65, d.f. = 2, p < 0.01) and by a species in relation to feeding habits. Bray abundance (H = 21.56, d.f. = 2, p < 0.01) among Curtis similarity matrices were constructed from bait types. (1) seasonal data on species abundance for the Thirteen species (39.40%) were considered 3 kinds of baits, excluding months with fewer to have generalist habits according to Levins’ than 10 individuals to minimize bias, and (2) from standardized index of niche breadth, and they a Morisita-Horn data matrix on niche overlap represented 15.48% of the total number of between species’ feeding habits. Due to the great captured individuals (with an average number heterogeneity in initial values, data for species of individuals per species of 234.61 ± 246.50). abundance were square root-transformed to Four species (12.12%) could not be classified homogenize the variances (Filgueiras et al. 2009). into food categories because the number of Ordination analyses (nonmetric multidimensional individuals (n < 15) was insufficient. Other species scaling [NMDS]) were performed using the (n = 16) were classified as having specialist food program Primer 6 (Clarke and Gorley 2005). The associations in this study. Of these, 14 species dimensional configuration of NMDS was evaluated were coprophagous and represented 79.25% by the level of stress, which ranged 0-1. of the total number of captured individuals (with Kruskal-Wallis tests, conducted with the an average number of individuals per species program PAST 2.02 (Hammer et al. 2001), were of 1115.21 ± 1525.52); another 2 species were performed to determine possible differences in necrophagous and represented 15.48% of the total richness and abundance between the kinds of bait number of captured individuals (with an average used. A two-way analysis of variance (ANOVA) number of individuals per species of 511.5 ± test, conducted in BioEstat 5.0 (Ayres et al. 2007), 64.34). No species showed saprophagy as the Zoological Studies 51(4): 429-441 (2012) 433 preferential feeding habit. Although classified as concise group, and neither did the 2 necrophagous specialists, all of these species were attracted to species. Generalist and necrophagous species more than 1 kind of bait. Trophic associations were widely scattered across the graph, and were consistent among seasons. most were statistically distant from coprophagous According to the ordination analysis species. conducted on food niche overlap (the simplified Dichotomius Hope, 1838, Eurysternus index of Morisita-Horn), scarabaeine species Dalman, 1824, Onthophagus Latreille, 1802, and (n > 15) with coprophagous feeding habits Ontherus Erichson, 1847, included a large group formed 2 clear groups. Generalist species with of coprophagous species with low food niche high values of niche overlap (Fig. 2) formed no overlap. The 2nd group of coprophagous species

Table 1. Numbers of individuals of species of the Scarabaeinae captured with pitfall traps baited with rotten banana (RB), rotten meat (RM), and human excrement (HE) in forest fragments in Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and Apr. 2010. %, Percentage of the total captured; BA, standardized index of Levins niche breadth for species with > 15 individuals. TH, trophic habit of the species (C, coprophagous; N, necrophagous; G, generalist; IN, insufficient number of individuals)

Bait Species Total % BA TH RB RM HE

Ateuchus aff. carbonarius (Harold, 1868) 0 0 1 1 0.01 - IN Ateuchus aff. robustus (Harold, 1868) 0 7 61 68 0.35 0.227 C Canthidium aff. dispar Harold, 1867 133 183 152 468 2.38 0.974 G Canthidium moestum Harold, 1867 10 30 12 52 0.26 0.682 G Canthidium aff. trinodosum (Boheman, 1858) 200 662 4061 4923 24.99 0.214 C Canthidium sp. 62 121 863 1046 5.31 0.217 C Canthon amabilis Balthasar, 1939 53 125 71 249 1.26 0.821 G Canthon chalybaeus Blanchard, 1845 46 270 117 433 2.20 0.557 G Canthon latipes Blanchard, 1845 100 554 2577 3231 16.40 0.250 C Canthon lividus Blanchard, 1845 97 422 167 686 3.48 0.592 G Canthon aff. luctuosus Harold, 1868 60 232 210 502 2.55 0.741 G Canthon oliverioi Pereira and Martínez, 1956 0 5 75 80 0.41 0.133 C Canthon quinquemaculatus Castelnau, 1840 16 366 84 466 2.37 0.269 N Coprophanaeus milon (Blanchard, 1845) 4 24 13 41 0.21 0.604 G Coprophanaeus saphirinus (Sturm, 1826) 27 366 164 557 2.83 0.460 N Deltochilum brasiliense (Castelnau, 1840) 5 9 10 24 0.12 0.898 G Deltochilum morbillosum Burmeister, 1848 0 17 14 31 0.16 0.981 G Deltochilum rubripenne (Gory, 1831) 40 224 233 497 2.52 0.664 G Deltochilum sculpturatum Felsche, 1907 2 10 5 17 0.09 0.620 G Dichotomius aff. acuticornis (Luederwaldt, 1930) 5 7 14 26 0.13 0.752 G Dichotomius assifer (Eschscholtz, 1822) 36 152 2817 3005 15.25 0.067 C Dichotomius nisus (Olivier, 1789) 2 4 22 28 0.14 0.278 C Eurysternus aeneus Génier, 2009 0 0 1 1 0.01 - IN Eurysternus caribaeus (Herbst, 1789) 11 70 1361 1442 7.32 0.060 C Eurysternus parallelus Castelnau, 1840 2 9 122 133 0.68 0.091 C Homocopris sp. 0 0 2 2 0.01 - IN Ontherus azteca Harold, 1869 1 10 32 43 0.22 0.322 C Ontherus sulcator (Fabricius, 1775) 6 69 553 628 3.19 0.135 C Onthophagus catharinensis Paulian, 1936 4 5 499 508 2.58 0.018 C Onthophagus aff. tristis Harold, 1873 4 17 335 356 1.81 0.063 C Phanaeus splendidulus (Fabricius, 1781) 0 7 18 25 0.13 0.676 G Sulcophanaeus rhadamanthus (Harold, 1875) 0 0 4 4 0.02 - IN Uroxys aff. terminalis Waterhouse, 1891 7 15 104 126 0.64 0.216 C

Number of individuals 933 3,992 14,774 19,699 Number of species 25 29 33 33 434 Silva et al. – Attractiveness of Different Baits to the Scarabaeinae comprised 2 species of Canthidium Erichson, Scarabaeinae were attracted to human excrement 1847, 1 Ateuchus Weber, 1801, and 1 Canthon (Fig. 4). Species captured in rotten meat more Hoffmannsegg, 1817. Although classified as frequently occurred in Nov. (43.14%) and Dec. coprophagous, high proportions of individuals of (21.84%), while those captured in the fermented these species were also captured in traps baited banana more frequently occurred in Dec. (23.79%) with rotten meat and rotten fruit. and Oct. (22.07%) (Fig. 4). These results are The 3-dimensional NMDS ordination plot (Fig. related to the greater richness and abundance of 3) shows clear clustering of species assemblages dominant and generalist species in this period. attracted to each bait type. Thus, the pattern of The lowest percentages of captures for meat species attracted to particular bait types remained and fruit bait in terms of individuals and species consistent throughout each month of the year occurred between June and Aug., and in July, no considered in the analysis. individuals occurred in these traps. These results Essentially, peaks in species richness and were apparently related to seasonal distributions of abundance coincided with the seasonal peak in temperature and precipitation in this region. rainfall (Sept. to Jan., but especially Oct. to Dec.) In total, 63.64% of species occurred in (Fig. 4), then declined with a reduction in rainfall all seasons of the year, 15.15% in 3 seasons, under high temperatures (Feb. to May) becoming and 12.12% in 2 seasons. The 2 latter groups, low from June to Aug. under the low rainfall and although present in more than 1 season, were temperatures of the cool dry season. more frequent in spring. Three species occurred Throughout the period, a majority of the in specific seasons: Ateuchus aff. carbonarius

2D Stress: 0.10 Deltochilum brasiliense Dichotomius aff. acuticornis Trophic guild Coprophagous Deltochilum rubripenne Coprophanaeus milon Generalist Deltochilum morbillosum Necrophagous Coprophanaeus saphirinus

Deltochilum sculpturatum

Canthon aff. luctuosus Canthon chalybaeus Phanaeus splendidulus Canthon amabilis Canthidium aff. trinodosum Canthon latipes Ateuchus aff. robustus Canthidium sp. Canthidium moestum

Canthon lividus

Canthidium aff. dispar Canthon oliverioi Dichotomius nisus Ontherus azteca Uroxys aff. terminalis Ontherus sulcator Dichotomius assifer Eurysternus parallelus Canthon quinquemaculatus Onthophagus aff. tristis Onthophagus catharinensis Eurysternus caribaeus

Fig. 2. Non-metric multidimensional scaling (NMDS) with Bray-Curtis similarity based on the Morisita-Horn index of food niche overlap showing the distribution of scarabaeine species according to each trophic guild (coprophagous, necrophagous, or generalist), captured by pitfall traps in forest fragments in Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and Apr. 2010. Species with fewer than 15 individuals were excluded. Zoological Studies 51(4): 429-441 (2012) 435

(Harold, 1868) occurred only in spring (Oct.) and (Q = 6.644, p < 0.05) and between spring and Eurysternus aeneus Génier, 2009 only in summer autumn (Q = 7.047, p < 0.01). (Dec.), while Sulcophanaeus rhadamanthus When abundances of the Scarabaeinae (Harold, 1875) was only collected in autumn (May). within different kinds of bait were compared among When the richness of the Scarabaeinae the seasons, significant differences among the bait was tested for the different kinds of bait among used (F = 22.446, d.f. = 2, p = 0.002) and seasons seasons, significant differences among bait types (F = 10.100, d.f. = 3, p = 0.01) were found (Fig. (F = 16.175, d.f. = 2, p = 0.004) and seasons 5B). According to the a posteriori Tukey’s test, (F = 17.581, d.f. = 3, p = 0.003) were found only human excrement, the average of which was (Fig. 5A). Significant differences in bait types, the highest, significantly differed from the bait of according to an a posteriori Tukey’s test, was fruit (Q = 9.187, p < 0.01) and meat (Q = 6.600, found between averages of human excrement and p < 0.01), while spring (highest average) fermented fruit (Q = 8.021, p < 0.01) and between significantly differed from autumn (Q = 6.580, human excrement and rotten meat (Q = 4.533, p < 0.05) and winter (Q = 6.883, p < 0.05). p < 0.05). Significant differences among seasons occurred between averages of spring and winter

3D Stress: 0.11 Bait Mar. Fruit

Meat

Excrement Aug. Jan. Aug. Mar. Apr. May Jan. June Feb. Apr. May July Aug. Mar. Dec. Dec. Sept. Nov. May Nov. Feb. Oct. Sept. Nov. Sept. Dec. Jan. Oct. Feb.

Oct.

Fig. 3. Non-metric multidimensional scaling (NMDS 3D plot) with Bray-Curtis similarity showing the distribution of the Scarabaeinae according to each kind of bait, captured by pitfall traps in forest fragments in Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and Apr. 2010. The symbols are the initials of the months. Months with fewer than 10 individuals were excluded from this analysis. 436 Silva et al. – Attractiveness of Different Baits to the Scarabaeinae

DISCUSSION scarabaeine assemblages in each type of baited trap throughout the study period. All species There was a clear distinction between the were classified into trophic groups with feeding levels of attraction of scarabaeine species to preferences that remained the same among the human excrement, rotten meat, and rotten fruit months and seasons. during the study period. Human feces was the The results of this study on the relative most attractive bait in terms of both the number attractiveness were as we expected, because the of individuals and species. Numbers consistently dung of omnivorous and herbivorous mammals is showed significant differences from the other the main food source used by most species of the bait types across months and seasons. These Scarabaeinae for nesting and feeding by adults differences occurred due to great changes in and larvae (Halffter and Matthews 1966, Halffter the composition, richness, and abundance of and Edmonds 1982, Hanski and Cambefort 1991,

(A) 100

80

60

40 Percentage (%)

20

0 May June July Aug. Sept. Oct. Nov. Dec. Jan. Feb. Mar. Apr. Fruit Meat Excrement

(B) 5000 90 600 35

80 30 500 4000 70 25 60 400 3000 50 20 300 40 15 2000 Number of individuals Mean temperature (°C) Precipitation (mm) Number of species 30 200 10 1000 20 100 5 10

0 0 May June July Aug. Sept. Oct. Nov. Dec. Jan. Feb. Mar. Apr.

Autumn Winter Spring Summer Autumn

Fig. 4. Monthly number of individuals and species of the Scarabaeinae, and proportion of individuals for each type of bait used in forest fragments of Santa Maria, Rio Grande do Sul, Brazil, between May 2009 and Apr. 2010, and distribution of environmental variables of mean temperature and precipitation during the study period. Zoological Studies 51(4): 429-441 (2012) 437

Simmons and Ridsdill-Smith 2011). In this study, sampled dung beetles using the same bait types all species and 75% of individuals were attracted used in this study, and they collected 84.68% of to human feces, confirming it to be one of the the total number of individuals and 89.28% of all most important bait for the effective capture of species in traps baited with human feces. Those Neotropical Scarabaeinae, both in forests and results suggest that the excrement of omnivorous pastures (Halffter and Matthews 1966, Falqueto et mammals potentially is of better quality or is more al. 2005, Larsen et al. 2006, Filgueiras et al. 2009, attractive than other kinds of dung (Cambefort Audino et al. 2011). and Hanski 1991, Hanski and Cambefort 1991). Other researchers obtained similar results. When different types of bait were used (excrement Fincher et al. (1970), Estrada et al. (1993), and vs. carrion vs. rotten fruit), it is probable that the Filgueiras et al. (2009) found higher proportions coprophagous eating habit of most collected of individuals in traps baited with excrement of species contributed to the high abundance in traps omnivorous mammals (such as humans) in relation baited with human feces. to other kinds of dung (carnivorous or herbivorous In relation to eating habits, the high number mammals). Silva et al. (2009) found higher of species considered coprophagous (14) demon- proportions of species and individuals in traps strated greatest attraction to bait with human baited with human excrement than in traps baited excrement compared to other kinds of bait with rotten chicken meat. Audino et al. (2011) (Larsen et al. 2006) and even to non-baited traps (Filgueiras et al. 2009, Silva 2011a). However, 13 species showed generalist eating habits, (A) and 2 others were specialist . The 35.0 Spring Summer Autumn Winter results were similar to those of Almeida and Louzada (2009) for the scarabaeine fauna of 30.0 different vegetation types captured with pitfall traps baited with human excrement and carrion in 25.0 the Cerrado in Carrancas, Minas Gerais, Brazil. Those authors also collected a large number of coprophagous species, some generalists, and a

Richness 20.0 smaller number of necrophagous species. Neither published results nor the present findings support 15.0 the hypothesis that assemblages of Neotropical Scarabaeinae include a higher proportion of 10.0 RB RM HE generalist species in relation to specialists (Halffter (B) and Matthews 1966, Halffter 1991). 11.0 Besides historical and evolutionary proce- sses (Halffter and Matthews 1966, Halffter 9.0 and Edmonds 1982, Halffter 1991, Hanski and Cambefort 1991, Davis et al. 2002, Davis 2009), 7.0 the high specialization to coprophagy in the Scarabaeinae seems to be related to the greater availability of mammal dung in the ecosystem Abundance 5.0 (Halffter and Matthews 1966), since there appear 3.0 to be fewer rotting fruits and carcasses of dead , and they may be seasonally and spatially limited (Howden and Young 1981, Louzada and 1.0 RB RM HE Lopes 1997). Baits However, necrophagy in the Scarabaeinae is considered particularly important in Neotropical Fig. 5. Two-way ANOVA analysis characterizing differences forests where the occurrence of large mammals is between species richness (A) and abundance (B) of the low (Halffter and Matthews 1966). For example, Scarabaeinae by season for each bait type (RB, rotten banana; Silva et al. (2008) sampled dung beetles using RM, rotten meat; HE, human excrement) in forest fragments of Santa Maria, Rio Grande do Sul, Brazil, between May 2009 pitfall traps baited with rotten meat and excrement and Apr. 2010. Values are presented as the mean ± standard of bovines across a field-forest and found deviation. a greater number of individuals in the 1st bait 438 Silva et al. – Attractiveness of Different Baits to the Scarabaeinae type. Furthermore, Silva (2011a) sampled dung been sufficiently attractive to species of the beetles in 2 non-native habitats and found greater Scarabaeinae in this region. Future studies will species richness in traps baited with human dung compare the attractiveness banana to fruits of jelly but greater abundance in traps baited with carrion. palm trees (butiá), since a significant number of In this study, only 2 necrophagous species were sarabaeine species are attracted to the fruits of found, Canthon quinquemaculatus Castelnau, these native palms (Pereira and Martínez 1956, 1840, and Coprophanaeus saphirinus (Sturm, Gill 1991, Halffter and Halffter 2009), which occur 1826), but 87.87% of the captured species were in forests of southern Brazil (Nunes et al. 2010). found in traps baited with rotten meat. A high number of species (13) were found to Canthon quinquemaculatus has a wide Neo- have generalist eating habits. According to Halffter tropical distribution and is common in animal and Matthews (1966), some species may vary their carcasses in the early stages of preference for different kinds of food resources (Martínez 1959, Halffter and Matthews 1966). according to its local availability. Many typically Although Martínez (1987) cited it as being exclu- coprophagous or copro-necrophagous species sively necrophagous, there are also records of its may use fruit as a food resource. In other cases, capture after attraction to the fetid smell liberated specialist saprophagous species are occasionally by recent cuttings of liana (Pereira and Martínez collected in traps baited with feces or carrion. In 1956). In contrast to this study, Martínez (1959) Neotropical forests, species being attracted to considered C. saphirinus a coprophagous species decaying fruit or plant material may be the result mainly found in the dung of herbivorous mammals of an evolutionary process in recent geological from southern Brazil to Bahia and also in Argentina times that is related to the great availability of and Paraguay (Martínez 1959, Arnaud 2002, this resource compared to the low diversity of Edmonds and Zídek 2010), where there were mammals and, consequently, the lower diversity of color variations among populations from different dung and carcasses (Halffter and Halffter 2009). localities (Edmonds and Zídek 2010). Although Although most species of the Scarabaeinae classified as necrophagous, these 2 species which are attracted to rotten fruit are also also occurred in human excrement and rotten captured in feces and carrion, some species banana. Due to the less-frequent occurrence of of Onthophagus and Canthidium may feed carcasses compared to excrement, the use of predominantly or exclusively on this resource (Gill other food resources (feces or fruit) by specialist 1991, Halffter and Halffter 2009), while species of necrophagous species appears to be a process other typically copro-necrophagous groups (such of maintaining themselves in periods when their as Canthon, Deltochilum Eschscholtz, 1822, and preferred food is unavailable. These results are Dichotomius) are often captured or attracted by in line with the findings of Halffter and Matthews rotten or fermented fruit (Pereira and Halffter 1961, (1966) who asserted that necrophages are not Halffter and Halffter 2009). exclusively necrophagous, since the species may Thus, trophic generalization or the use of use more than 1 kind of dietary resource according more than 1 type of food resource decreases to its availability in the ecosystem. Coprophagous competition for scarce and ephemeral food such species that preferentially use human excrement as excrement, animal carcasses, and rotten plant also show a greater tendency to occasional matter (Halffter and Halffter 2009). Apparently, necrophagy (Halffter and Mathews 1966). As trophic generalization can also give a species a assumed by Falqueto et al. (2005), species that wider use of the environment, while specialization use rarer resources than excrement (such as tends to limit the occupation of new ecosystems carrion and rotten fruit) seem to have a higher where the preferred food is not available. The trophic generality. ability to utilize alternative foods would have Mature and decaying fruit is particularly contributed to the high diversity of the Neotropical attractive to a variety of species of the Scarabaeinae (Halffter and Halffter 2009). Scarabaeinae (Gill 1991). In this study, 75.75% of In this study, human feces was the most species represented by only 4.74% of individuals attractive bait, differing significantly from carrion occurred in traps baited with rotten banana, and rotten banana in both species richness and although always in lower abundances than those abundance of the Scarabaeinae. Coprophagous found in human excrement and rotten meat. As species showed the greatest abundance and bananas are not native to subtropical forests distinctly differed in patterns of attraction to of southern Brazil, this bait type might not have bait compared to generalist and necrophagous Zoological Studies 51(4): 429-441 (2012) 439 species. Differences between patterns of attra- Dambros VS, SM Eisinger, TS Canto-Dorow. 2004. Legumi- ction to the bait persisted throughout the entire nosae do Campus da Univ. Federal de Santa Maria, Rio Grande do Sul, Brasil. Ciência e Natura 26: 43-60. (in study period. Species captured during periods of Portuguese with English summary) low temperatures were frequently coprophagous Davis ALV. 2009. Historical origin, evolutionary timescale, taxa that showed the highest abundances in this and its drivers. In CH Scholtz, ALV Davis, U Kryger, eds. study. Generalist species always occurred at Evolutionary biology and conservation of dung beetles. lower abundances, and most of them were found Sofia, Bulgaria: Pensoft Publishers, pp. 335-337. Davis ALV, CH Scholtz. 2001. Historical versus ecological in greater numbers in traps baited with rotten meat factors influencing global patterns of scarabaeine dung and at greater frequencies during the spring. beetle diversity. Divers. Distrib. 7: 161-174. Davis ALV, CH Scholtz, TK Philips. 2002. Historical biogeo- Acknowledgments: The 1st author thanks the graphy of scarabaeine dung beetles. J. Biogeogr. 29: Coordenação de Aperfeiçoamento de Pessoal 1217-1256. Edmonds WD, J Zídek. 2010. A taxonomic review of the de Nível Superior (CAPES) for the scholarship, genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Suzane Saldanha for improving the English Scarabaeidae: Scarabaeinae). Insecta Mundi 129: 1-111. version of the manuscript, and Franciéle Estrada A, G Halffter, R Coates-Estrada, DA Meritt Jr. 1993. Garcês for assistance during fieldwork. This Dung beetles attracted to mammalian (Alouatta work was partially funded by the Fundação de palliata) and (Nasua narica) dung in the tropical rain forest of Los Tuxtlas, Mexico. J. Trop. Ecol. 9: 45-54. Amparo à Pesquisa do Estado de Mato Grosso Falqueto SA, FZ Vaz-de-Mello, JH Schoereder. 2005. Are (FAPEMAT 570847/2008 and 447441/2009) fungivorous Scarabaeidae less specialist? Ecol. Aust. 15: and Conselho Nacional de Desenvolvimento 17-22. Científico e Tecnológico (CNPq 151603/2007-3 Filgueiras BKC, CN Liberal, CDM Aguiar, MIM Hernández, L and 304925/2010-1). Thanks are also due to Iannuzzi. 2009. 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